Abstract
Acute rerupture after coil embolization is defined as rerupture within three days after treatment; its prognosis is worse than that of rebleeding at other time periods. However, to date, little is known about complications during the acute phase. Therefore, we used the PubMed database to perform a review of acute rerupture after coil embolization of ruptured intracranial saccular aneurysms and increase our understanding. After reviewing the complications, we found that the cause of acute rerupture is unclear, but the following risk factors are involved: incomplete occlusion of the initial aneurysm, the presence of a hematoma adjacent to a ruptured aneurysm, an aneurysmal outpouching, poor Hunt-Hess grade at the time of treatment, and the location of the aneurysm in an anterior communicating artery. In addition, intraoperative rupture is a non-negligible cause. Acute rerupture after coil embolization mainly occurs within the first 24 hours after the procedure. Brain computed tomography is the gold standard for diagnosing acute rebleeding of a coiled aneurysm. For acute rerupture after coil embolization, prevention is critical, and complete occlusion of the aneurysm in the first session is the best protection against acute rebleeding. In addition, a restricted postembolization anticoagulation strategy is recommended for patients with high-risk aneurysms. For patients with an adjacent hematoma, surgical clipping is recommended. Most patients present no changes immediately after acute rebleeding because of their poor condition. However, surgical or endovascular treatments can be attempted if the patient is in an acceptable condition. Even so, the outcomes are typically unsatisfactory.
Keywords: Intracranial aneurysm, acute rerupture, coil embolization, review
Introduction
Currently, coil embolization is a safe and effective procedure for the treatment of ruptured intracranial aneurysms.1–3 As endovascular therapy becomes more commonly used for treating aneurysms, the prevalence of periprocedural complications is expected to rise accordingly. 4 The main causes of morbidity and mortality are thromboembolisms, intraprocedural aneurysm ruptures, and postprocedural aneurysmal reruptures. 5 Among these complications, postprocedural aneurysmal reruptures are often fatal or disabling. 6
Reruptures can be divided into early and late types based on the timing of the postprocedural aneurysmal rerupture. 7 Early rerupture is defined as a bleeding event within 30 days after coiling accompanied by worsening of the patient’s condition; it can be further divided into acute (within three days), subacute (4–14 days), and delayed (15–30 days) depending on the timing of the rerupture after coil embolization.8,9 Among all reruptures, acute reruptures have the worst outcome, with a mortality rate of up to 75%. Because of poor prognosis, acute rebleeding is different from rebleeding at other time periods. Therefore, this paper focused on discussing reruptures during the acute phase after coil embolization.
Acute rerupture after coil embolization is not uncommon among patients with dissecting aneurysms, blood blister-like aneurysms, fusiform aneurysms, and pseudoaneurysms; these aneurysms have different etiological and anatomical characteristics than saccular aneurysms, which are also at high risk of rerupture. Therefore, coil embolization is often unfeasible.10–12 Instead, these aneurysms are often treated by endovascular sacrifice of the parent vessel and were excluded from our paper. 13 The present paper evaluated acute rerupture after coil embolization of only saccular or berry aneurysms.
To date, little is known about acute rerupture after coil embolization of ruptured intracranial saccular aneurysms, as acute rerupture is rarely investigated. No overall and systematic review of acute rerupture after coil embolization is currently available. Thus, in this paper, we used the PubMed database to perform a review of acute rerupture after coil embolization of ruptured intracranial saccular aneurysms to increase our understanding.
Incidence
Rerupture is uncommon after a ruptured intracranial saccular aneurysm has been treated with either coil embolization or surgical clipping. The International Subarachnoid Aneurysm Treatment (ISAT) found a 1.7% risk of rerupture in the first year after surgery, and the rerupture rate has gradually trended downward over time. 14 Half of all cases of reruptured aneurysms occur during the acute stage (the first three days) after coiled treatment, and there are major consequences. 15 However, little is known about the exact incidence of acute rerupture after coil embolization of ruptured intracranial saccular aneurysms; the rerupture rate may be 1.0% to 3.6%.8,16
Owing to the different patient populations, the incidence differs among studies. For example, in the 2015 study by Chang et al., the incidence of acute rerupture after coil embolization was 2.1%. 17 In another large case study by Kang et al. in 2010, the incidence of acute rerupture was approximately 1.0%. 18 In the study by Jartti et al. in 2010, the incidence of acute rerupture was 3.6%. 8 Therefore, we expect that a study with a larger sample size would better estimate the incidence of acute rerupture after coil embolization of ruptured intracranial saccular aneurysms.
Timing distribution
Most reruptures after coil embolization of ruptured intracranial saccular aneurysms occur in the acute stage within three days of the initial embolization. For example, in 2012, Cho et al. reported that 10 patients experienced rerupture after coil embolization, and all of the events occurred within three days. 9 However, the exact timing distribution of the acute stage differs among the different studies. For example, Kang et al. reported in 2010 that six out of 591 patients experienced acute rerupture, and the reruptures occurred from 8 to 23 hours post-procedure. 18 Chang et al. reported in 2015 that seven out of 330 patients experienced acute rerupture, which occurred from 5 to 65 hours after coil embolization; in five of these seven patients with rebleeding, the events occurred approximately 24 hours after embolization. 17 Thus, for acute rerupture after coil embolization, most events occur within the first 24 hours. Therefore, more caution should be taken within one day of coil embolization of ruptured intracranial saccular aneurysms.
Risk factors
Many risk factors are involved in acute rerupture after coil embolization of ruptured intracranial saccular aneurysms, including incomplete embolization, use of anticoagulant agents, the presence of an intracranial hematoma (ICH) and a high Hunt-Hess (HH) grade, the presence of a bleb, and aneurysm location or size. 19 The risk factors of acute rerupture are different from those of late rebleeding; late rerupture of aneurysms is mainly due to aneurysmal recanalization, which is caused by coil compaction or aneurysmal growth.9,20
Incomplete embolization
Incomplete embolization of ruptured intracranial saccular aneurysms is the strongest risk factor for acute rebleeding, and the degree of coil occlusion is determined by the modified Raymond Classification. 21 In the Cerebral Aneurysm Rerupture After Treatment (CARAT) study, an initial occlusion grade <70% was a strong predictor of acute rerupture; the loosely coiled area of the aneurysm could lead to the ruptured point of the aneurysm and is a likely mechanism of rebleeding. 22
Although incomplete embolization can result in acute rerupture, complete occlusion does not always prevent rerupture. For example, in 2003, Asgari et al. reported that the rate of recurrent hemorrhage after complete occlusion of an aneurysm was 0.9% in their coiling group; moreover, some ruptured aneurysms reruptured during the acute stage after coil embolization. 23 Thus, other risk factors are involved in acute rerupture after coil embolization.
Anticoagulants
Stent therapy has been considered an advancement in endovascular aneurysm coiling because it allows for the treatment of wide-necked aneurysms; however, stent-assisted coiling requires dual-antiplatelet therapy,24–26 which can cause acute rerupture after coil embolization. Acute recanalization may occur with the spontaneous resolution of thrombi through the inserted coil loops, which makes dual-antiplatelet therapy a possible mechanism of acute rebleeding despite satisfactory occlusion of the aneurysms. Thus, the use of dual-antiplatelet therapy, which is usually administered after coiling to prevent thromboembolic complications, is a risk factor. 27
Presence of an adjacent ICH and a high HH or Fisher grade
Several studies have shown that the presence of an ICH on the initial computed tomography (CT) and an HH grade 3–5 before coiling were risk factors for acute reruptures after coil embolization of intracranial saccular aneurysms.8,9 Patients with a high HH or Fisher grade often have an ICH,28,29 and when there is an adjacent ICH, a thrombosed pseudoaneurysm may hide in the adjacent ICH and avoid detection by digital subtraction angiography (DSA). During coil embolization, the pseudoaneurysm cannot be coiled. Thus, thrombosed pseudoaneurysms inside the ICH may cause acute reopening and rebleeding.
Other risk factors
Additional risk factors include the presence of a bleb or an outpouching of an irregular aneurysm, aneurysm location and size, and intraoperative rupture. 30
Blebs or outpouchings in aneurysms most likely indicate an especially weak portion of the aneurysm dome and are often the site of initial rupture. 19 Some interventionists attempt to avoid inserting the coil into the bleb out of fear of procedural rupture; thus, the risk of coil compaction may be high. 2 Blebs or outpouchings are, thus, a risk factor for acute rerupture after coil embolization.
The location and size of the aneurysm may be additional risk factors. For example, in the 2005 study by Sluzewski and van Rooij and the 2009 study by Willinsky et al., the authors considered that the anterior communicating artery (ACoA) has a predilection for acute rerupture after coil embolization, followed by middle cerebral artery (MCA) and posterior communicating artery (PCoA) aneurysms. Aneurysms in these locations may rerupture because of hemodynamic stress.16,31 Another possible explanation is that rupture of an ACoA and MCA aneurysm is often associated with an adjacent ICH.
In addition, a meta-analysis showed that aneurysm size is an important risk factor for aneurysmal acute rebleeding. 32 Some studies consider an aneurysm size of less than 6 mm as an independent risk factor for acute rebleeding.16,31 However, the influence of the aneurysm location and size on acute rebleeding lacks peer-reviewed evidence. Inoperative rupture during coil embolization may be a risk factor for acute rerupture because intraoperatively extruding a mass through a transparent aneurysmal wall increases the instability of the aneurysm; however, this also requires peer-reviewed evidence.
The risk factors of acute rerupture after coil embolization are summarized in Table 1.
Table 1.
Risk factors and treatment of rerupture after endovascular coil embolization.
| Risk factors | Key point |
|---|---|
| Incomplete embolization | Incomplete embolization of a ruptured intracranial saccular aneurysm is the strongest risk factor associated with acute rebleeding. An initial occlusion grade <70% is a strong predictor of acute rerupture. Therefore, complete occlusion of an aneurysm in the first session is the best preventive measure against rerupture. |
| Anticoagulants | Dual-antiplatelet therapy can cause acute rerupture after coil embolization because acute recanalization may occur following the spontaneous resolution of thrombi through the inserted coil loops. Therefore, reduction of the routine postprocedural anticoagulation therapy may be beneficial, except in patients who may be at risk for thromboembolic complications based on patient- and procedure-related factors. |
| Presence of an adjacent ICH | When an adjacent ICH is present, a thrombosed pseudoaneurysm may hide in the adjacent ICH and cannot be observed on DSA. Thus, during endovascular embolization, the pseudoaneurysm cannot be coiled, and the thrombosed pseudoaneurysms inside the ICH may cause acute reopening and rebleeding. Reducing the routine postprocedural anticoagulation therapy may be beneficial. In addition, if acute follow-up angiograms can be performed prior to rebleeding, the angiogram might help prevent rebleeding. |
| Presence of a bleb | Blebs or outpouchings in aneurysms most likely indicate an especially weak portion of the aneurysm dome and are often the site of initial rupture. If coiling of the bleb is avoided due to fear of intraprocedural rupture, the risk of coil compaction may be high. Thus, to prevent rebleeding, the bleb should be coiled with caution. |
| Location of aneurysm | The anterior communicating artery aneurysm has a predilection for acute rerupture after coiling embolization, followed by middle cerebral artery and posterior communicating artery aneurysms. Aneurysms in these locations may rerupture due to hemodynamic stress or its association with an adjacent ICH. Thus, increased attention should be paid to these aneurysms to detect rerupture, especially aneurysms with an adjacent ICH. |
| Size of aneurysm | An aneurysm size of less than 6 mm may be considered an independent risk factor for rebleeding. Thus, for small aneurysms, complete coiling should be recommended. |
| Inoperative rupture | Because intraoperatively extruding a mass through a transparent aneurysmal wall increases the instability of the aneurysm, intraoperative rupture during coil embolization should be a risk factor. Therefore, complete coiling and reducing the routine postprocedural anticoagulation therapy may be beneficial. |
ICH: intracranial hematoma; DSA: digital subtraction angiography.
Clinical manifestation
Acute rerupture after coil embolization of ruptured intracranial saccular aneurysms is defined as clinical deterioration, including neurological deterioration, sudden severe headache, and a sudden fluctuation of vital signs in the acute stage (i.e. within three days). 17 However, it can be difficult to identify worsening clinical conditions when the patient is already in a coma or in poor condition.
The symptoms of acute rerupture differ from those of late rerupture. Patients with late reruptures recover well from the first subarachnoid hemorrhage (SAH); the late reruptures are similar to new SAHs. However, patients with acute rerupture after coil embolization suffer at least twice from SAH in a short period; thus, these patients are often in worse clinical condition. 30
Imaging examination
Brain CT is the gold standard for diagnosing acute rebleeding of a coiled aneurysm. Acute rerupture of intracranial aneurysms should be defined as a significant increase in the amount of SAH in the acute stage (i.e. within three days) after coil embolization compared with that in an immediate postprocedural brain CT. 33 However, in patients with an adjacent ICH, an increased or a newly developed ICH without increased SAH is not considered a rebleeding event.
In addition to CT, the use of contrast-enhanced magnetic resonance angiography (MRA), non-contrast-enhanced, zero echo time MRA and time-of-flight MRA may help identify an intrasaccular clot or partial thrombosis in some special coiled aneurysms.34,35 The new iterative metal artifact reduction algorithm enhances non-enhanced computed tomography angiography (CTA) quality after coiling. 36 In addition, CTA by gated data reconstruction and by shifting the reconstruction window is a promising technique for reducing artifacts. 37 These images may be helpful for patients who have undergone coil embolization.
Prevention and treatment
Prevention
The best preventive measure against acute rerupture after aneurysm coiling is complete occlusion of the aneurysm in the first session. 38 In addition, reducing postprocedural anticoagulation therapy may be beneficial in some cases with an ICH, except in patients who may be at risk for thromboembolic complications based on patient- and procedure-related factors. 30 Patients with an adjacent ICH and poor clinical grade should undergo close clinical and radiological examination, and the possibility of acute rerupture should be kept in mind.
In addition, the new lumen of an aneurysm may be visible if acute follow-up angiograms are performed prior to rebleeding within three days after coil embolization; thus, angiograms may help prevent rebleeding, particularly in patients with an ICH. However, daily angiograms are usually not possible and cannot be justified for the detection of an uncommon complication in every individual treated with coil embolization.
Treatment
Most patients cannot receive immediate surgical or endovascular treatments after acute rebleeding because of poor conditions. However, if acute rerupture of a coiled aneurysm occurs in a patient in an acceptable condition, a repeat cerebral angiogram may be required; additionally, repeat coiling or parent artery occlusion can be attempted. 39 In addition, among patients with an ICH who need a decompressive craniotomy, an immediate craniotomy should be considered for exploration and additional clipping if possible. Among all hematomas, patients with a perisylvian hematoma caused by an MCA aneurysm can achieve good outcomes; thus, more attention should be given to these patients.19,40
Prognosis
A shorter time between rebleeding and coil embolization correlates with worse patient prognosis; thus, acute reruptures have the worst prognosis due to multiple SAHs in a short duration. 7 Although the acute rebleeding rate after coiling may seem low, the outcomes after acute rebleeding are serious. 41 Johnston et al. reported in 2008 that 19 out of 1001 patients experienced postprocedural rerupture, with a median time to rerupture of three days, and 58% of the reruptures resulting in death. 22 In 2010, Kang et al. reported that six out of 591 patients experienced acute rerupture and that the rebleeding occurred within 24 hours in all cases; four of these six patients showed poor clinical courses, either dying or recovering with severe disability. 18
Thus, acute rerupture after coil embolization is often fatal or disabling, and the prognosis is poor. Even among patients who underwent repeat surgical or endovascular treatments, there were no satisfactory outcomes.
Typical cases
In this paper, we present two cases of acute rerupture after coil embolization of ruptured intracranial saccular aneurysms. Case 1 was an ACoA aneurysm with an adjacent ICH; the aneurysm was treated by stent-assisted coiling, and dual-antiplatelet therapy was administered. The patient suffered acute rerupture within one day and died two days later. Case 1 supports the hypothesis that an adjacent ICH and dual-antiplatelet therapy are risk factors for acute rebleeding.
Case 2 was a PCoA aneurysm. The patient was in good preoperative condition; the aneurysm was also treated by stent-assisted coiling, and dual-antiplatelet therapy was administered. During coil embolization, an inoperative rupture occurred despite satisfactory embolization as determined by angiography. The patient suffered acute rerupture within three hours and died one day later. Case 2 supports the hypothesis that intraoperative rupture is a risk factor for acute rebleeding following coil embolization.
Images of case 1 and case 2 are provided in Figures 1 and 2.
Figure 1.
Images of case 1. (a) and (b) CT showing the SAH and hematoma in the interhemispheric fissure; the first SAH is depicted. (c) and (d) CTA showing the ACoA aneurysm; the aneurysm was wide necked, and the right A1 was dysplastic. (e) and (f) CT showing that the second SAH was larger than the first SAH. (g) Three-dimensional-DSA clearly showing the ACoA aneurysm. (h) DSA showing the embolization projection degree. (i) and (j) DSA showing that the aneurysm was coiled with the assistance of a stent. (k) and (l) CT showing the acute rebleeding of the coiled ACoA aneurysm within one day of coil embolization. CT: computed tomography; SAH: subarachnoid hemorrhage; CTA: computed tomography angiography; ACoA: anterior communicating artery; DSA: digital subtraction angiography.
Figure 2.
Images of case 2. (a) and (b) CT showing the SAH, mainly focusing on the cisterna ambiens. (c) and (d) CTA and 3D-DSA showing the PCoA aneurysm; the aneurysm was wide necked. (e) DSA showing the embolization projection degree. (f) DSA showing that the aneurysm was coiled with the assistance of a stent. (g) DSA showing the intraoperative rupture. (h) and (i) DSA showing that the intraoperative rupture was controlled and that the aneurysm was completely embolized. (j) X-per CT of DSA showing the SAH and extravasation of the contrast medium. (k) and (l) CT showing acute rebleeding within three hours of coil embolization. CT: computed tomography; SAH: subarachnoid hemorrhage; CTA: computed tomography angiography; 3D-DSA: three-dimensional digital subtraction angiography; PCoA: posterior communicating artery.
Summary
Although acute rerupture after coil embolization is extremely rare, it is a possible complication of coil embolization of a ruptured saccular aneurysm, even when successful embolization is determined by angiography. The cause of acute rerupture is unclear, but some risk factors have been identified, including incomplete initial aneurysm occlusion as well as the presence of either an ICH adjacent to a ruptured aneurysm or an aneurysmal outpouching, poor HH clinical condition at the time of treatment, and the location of the aneurysm within the ACoA. We consider intraoperative rupture as a non-negligible cause of acute rebleeding.
Patients with an acute rerupture have a very poor prognosis; therefore, prevention is crucial. The best preventive measure against acute rerupture after aneurysm coiling is complete occlusion of the aneurysm in the first session. In addition, a more restricted postembolization anticoagulation strategy in patients with high-risk aneurysms may prevent the occurrence of rerupture. More attention should be paid to patients with a hematoma adjacent to a ruptured aneurysm, and surgical clipping is recommended instead of endovascular treatment.
Most patients exhibited no immediate changes after acute rebleeding because of their poor condition, but if the patient is in an acceptable condition when acute rerupture of a coiled aneurysm occurs, surgical or endovascular treatments can be attempted. However, even among patients who underwent repeat surgical or endovascular treatment, there were no satisfactory outcomes.
Limitation
Currently, literature on acute rerupture after coil embolization is lacking, and there are limited small case reports. Therefore, peer-reviewed evidence is insufficient. Nevertheless, we sought to review the limited literature regarding these cases. Although there was no peer-reviewed evidence, the information presented in this paper may be helpful to neurosurgeons.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
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